Due to the current lack of genetic tools in the anurans, I applied a comparative evolutionary approach to understand if the multi-glomerular projection pattern of individual RN axons might be more relevant in the animal kingdom. Single RN tracings in vertebrate species are quite scarce and the field mostly relies on the rodent data. To test, whether the multi-glomerular RNs might be a shared trait of amphibia in general, I labelled and analyzed axons of individual RNs in the neotenic Axolotl salamander
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(Figure 8A). Multi-glomerular RN projections might be even more common in this species and possibly other urodele amphibians (Chapter 5; Weiss et al., 2020). The axons innervated even more glomeruli than in the anurans and I only found a single uni-glomerular axon. The data from the Axolotl supports the idea that multi-glomerular RN axon projections might be common and possibly conserved among all urodele and anuran amphibians (Figure 8).
Figure 8 Uni- and multi-glomerular wiring in olfactory systems.
A) The distribution of uni- and multi-glomerular RN axons and projection neuron dendrites is shown. The amphibians in particular show a mix of both uni-glomerular and multi-glomerular axonal/dendritic patterns (*Chapter 5). B) Two potential wiring logics for the main olfactory system of anurans is depicted. In a labelled line scenario (left), the multi- and uni-glomerular projections are mirrored on the post- and presynaptic side.
Projection neurons thus only get input from a particular allele of olfactory receptor (homo-typic input) In the alternative wiring scenario (right), presynaptic signal could be diverged presynaptically and projection neurons could receive hetero-typic input on their multiple dendrites. Similarly, a single glomerulus could contain information from different receptor neuron populations. Other scenarios are possible. C) Multi-glomerular RN axonal projections and multi-tufted projection neurons are also found in the antennal lobe of the locusts (Ignell
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Contrastingly, individual RN projections in the sea lamprey and the adult zebrafish were almost exclusively uni-glomerular (Weiss et al., 2020). This is again in accordance with the uni-tufted morphology of the projection neurons of the respective species (Fuller et al., 2006; Green et al., 2013;
Figue 8A). It is to note however, that these two species of course don’t fully account for the variability of fishes and their olfactory systems (Hamdani and Døving, 2007; Olivares and Schmachtenberg, 2019) and because of the small sample size, it is possible that multi-glomerular projections are present in these species as well, although possibly less abundant. The presence of multi-glomerular projection neurons in other ray finned fishes like the goldfish suggests, that the uni-glomerular zebrafish pattern could be a derived trait and that other fish species could also have multi-glomerular RN axon projections. Similarly, projection neurons in the MOB of reptiles are also usually multi-glomerular (Dryer and Graziadei, 1994). More comparative data is necessary to understand which of the two patterns is the ancestral trait in vertebrates, or if they are generally present in parallel.
It is remarkable how similar the cellular composition of the insect and vertebrate system has evolved.
In general, RNs in insects also innervate a single glomerulus and individual projection neurons receive information from a single glomerulus (Couto et al., 2005; Hansson and Stensmyr, 2011; Yan et al., 2020). However, several deviations from this norm exist, reminiscent of the pattern I found in the anurans. In orthopteran insects, the antennal lobe consists of about 1000 microglomeruli, which are innervated by multi-glomerular RN projections (Ernst et al., 1983; Ignell et al., 2001; Figure 8C). The morphology of the projection neurons also exhibits the multi-glomerular pattern (Ignell et al., 2001).
This trait is hypothesized to be derived and not ancestral in orthopterans, because it gradually developed in this particular clade of insects and is absent in the most basal species (Ignell et al., 2001).
In some crustaceans, individual RN projections similarly innervate several glomeruli in the olfactory lobe e.g. in the terrestrial hermit crab (Tuchina et al., 2015) and the spiny lobster (Schmidt et al., 1992) and a single projection neuron often receives input of up to 80% of all glomeruli (Wachowiak and Ache, 1994). Neither the pre- nor the postsynaptic pattern is functionally explained so far.
A recent study on the functions of projection neurons in the macro-glomerular complex of moths showed that some projection neurons receive input from a single glomerular compartment of the complex while others are multi-glomerular (Lee et al., 2019; Figure 8C). The macro-glomerular complex has been shown to be involved in pheromone detection and Lee and colleagues found evidence, that the multi-glomerular projection neurons are showing different responses to pheromonal blends than their uni-glomerular counterparts and might thus be part of a non-redundant processing channel (Lee et al., 2019). This example shows that both connectivity pattern alongside could be a strategy to extract different aspects of olfactory information. To what extend this is transferrable to the orthopterans, the anurans or the rodent AOB is at this point unclear.
et al., 2001). In the pheromone-detecting macro-glomerular complex of the moth, uni- and multi-glomerular projection neurons constitute different functional processing channels (Lee et al., 2019). The stars indicate results obtained in the course of this thesis.
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Summary
General similarities of the olfactory system from insects to mammals make it tempting to extrapolate from one species to the other. However, the olfactory system is remarkably adaptive and diversified among animal lineages and species occupying different ecological niches. The amphibians are a particularly interesting group of animals, since they are the descendants of the first land living vertebrates and still partially depend on water. In my thesis, I examined adaptive features of the olfactory system of anurans across different distantly related species and in different developmental stages.
• Anuran tadpoles have radiated into many different aquatic microhabitats and have adopted several different lifestyles and feeding habits. Nevertheless, I found that the organization of glomerular clusters in the MOB is remarkably conserved in anuran larvae, constituting a morphological and possibly functional blueprint for tadpole olfaction.
• Before the onset of metamorphosis, the main olfactory system of Xenopus consists of a sensory epithelium in the PC, which connects to the glomerular clusters in the vMOB. In this thesis, I showed that during metamorphosis, projections to the vMOB are gradually replaced by cells from the newly formed MC (adult ‘water nose’) until the metamorphotic climax.
Despite the complete rewiring, the vMOB retains its coarse functional organization and odorant-mediated behavior to waterborne stimuli is still present. In the terrestrial Dendrobates tinctorius, the glomerular clusters of the vMOB show signs of degeneration, possibly as a sign of less reliance on aquatic olfaction.
• During metamorphosis, cells in the larval PC are completely replaced to form the adult ‘air nose’. The new PC neurons project their axons towards a new glomerular projection field in the dMOB. I found that in the dMOB, RN projections from the left and right PC show a substantial amount of overlap, and individual glomeruli around the midline receive bilateral input. Postsynaptic projection neurons in the dMOB extend multiple primary dendrites to multiple glomeruli, putatively integrating bilateral sensory input. It remains to be shown, whether this particular pattern might be behaviorally relevant, e.g. in olfactory-guided spatial orientation.
• Single RN axons in vertebrates are generally believed to be unbranched and only innervate a single glomerulus in the MOB. In my thesis, I show that multi-glomerular projections of individual RNs are conserved among ecologically diverse anurans and are also present in the axolotl. In contrast, the sea lamprey and the zebrafish almost exclusively showed a uni-glomerular projection pattern. Axonal bifurcations seem to be an ancestral feature in amphibians, and are possibly more common among vertebrates, forming an alternative odorant processing channel.
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